Introduction
Darwin developed the theory of sexual selection to explain evolution of
traits, such as elaborated antlers or feathers, which by hampering
survival, and thus apparently contradicted his theory of natural
selection (Darwin 1859, 1871). Darwin’s solution highlighted the role of
such costly traits in reproductive competition: antlers help males to
win in combat over access to females, and colourful feathers make males
sexually more attractive. However, he also appreciated that sexual
competitiveness is likely to be associated with general health and
vigour, and thus sexual selection may be partly aligned with natural
selection (Darwin, 1859). In contemporary theory of sexual selection,
this is framed in terms of condition-dependence of sexual trait
expression, with condition being defined as a trait capturing genetic
variation in an individuals’ ability to acquire and effectively process
resources. This “genic capture” mechanism implies that individuals
which are better-adapted and/or less burdened with mutations, should be
more likely to reproduce and pass their genes to next generations
(Andersson, 1986; Rowe & Houle, 1996).
The degree to which sexual selection is aligned with natural selection
is likely to affect the risk of extinction. On the one hand, studies
manipulating opportunity for sexual selection experimentally have
demonstrated that sexual selection can help adaptation to a novel
environment (Long et al., 2012; Plesnar-Bielak et al., 2012; Grieshop et
al., 2016; Parrett & Knell, 2018), purge genetic load (Radwan, 2004;
McGuigan et al., 2011; Almbro &Simmons, 2014) and in consequence,
prevent extinction (Jarzębowska & Radwan, 2010; Plesnar-Bielak et al.,
2012; Lumley et al., 2015; Godwin et al., 2020) (but see e.g. Arbuthnott
& Rundle, 2012; Chenoweth et al., 2015, for counterexamples). On the
other hand, elaborated sexual traits may become a burden to survival,
especially during stress associated with environmental changes, which
can eventually lead to extinction (Kokko & Brooks, 2003). While
expression of condition-dependent sexually selected traits may be
supressed under environmental stress, thus alleviating their costs to
their bearers, genes underlying these traits may also have negative
pleiotropic effects in female productivity and survival (Harano et al.,
2010; Plesnar-Bielak et al., 2014; Łukasiewicz et al. 2020), which could
contribute to increased risk of extinction (Kokko & Brooks, 2003).
Comparative work yielded conflicting results: some studies reported
increased risk associated with elaboration of male sexually selected
traits (Doherty et al., 2003; Morrow & Pitcher, 2003; Martins et al.,
2018; Bro-Jørgensen, 2014), while others found no evidence for such
relationship (Morrow & Fricke, 2004). These apparent inconsistencies
can result from uncontrolled differences in the genetic diversity of
populations of their exposure to environmental stressors. This
possibility is highlighted by a recent study by Parrett et al. (2019),
who found that generally positive effect of sexually selected beetle
horns on survival is modulated by a degree of anthropogenic alteration
of the habitat. Additional confounding factors may include differences
in population sizes (Martinez-Ruiz & Knell, 2017) or in breadths of
ecological niches, which can be modulated by the degree of sexual
dimorphism (Bonduriansky, 2011; De Lisle & Rowe, 2015). Further
progress could be achieved by using an experimental evolution approach,
which have grossly contributed to our understanding of the contribution
of sexual selection to population fitness (see Cally et al., 2019 for
review). However, experimental evolution studies that measured
extinction rate so far primarily manipulated mating systems or sex ratio
(Plesnar-Bielak et al., 2012; Jarzębowska & Radwan, 2010; Parrett &
Knell, 2018; Goodwin et al., 2020), rather than expression of
exaggerated sexual traits. Thus, they cannot inform us on how evolution
of such traits affects the risk of extinction.
Here, we experimentally assess the risk of extinction associated with
the expression in males of a costly, sexually selected weapon under
environmental change (gradual increase in ambient temperature by
20C per generation). Our model species was the
male-dimorphic bulb mite Rhizoglypus robini , in which some males
(but not females) express a sexually selected weapon: thickened third
pair of legs. The weapon, expressed only in a fighter male morph is both
significantly heritable and costly to produce (Radwan, 1995; Smallegange
& Coulson, 2011). Part of the heritability could be due to higher load
of deleterious mutations preventing males from expressing costly weapon.
Indeed, comparison of inbreeding depression between inbred lines derived
from fighters and scramblers indicated that the load of deleterious
mutations is higher in the scramblers (Łukasiewicz et al., 2020). Thus,
purifying selection should be stronger in populations in which the male
weapon is present, possibly decreasing their risk of extinction.
Furthermore, condition-dependence of the weapon expression (Radwan,
1995; Smallegange, 2011) should ensure that its direct costs to males
can be plastically reduced under environmental challenge. However,
females from genetic lines nearly fixed for fighter morph were shown to
have lower fitness compared to lines nearly fixed for scrambler morph in
two independent populations (Plesnar-Bielak et al., 2014; Łukasiewicz et
al., 2020), indicating that genes associated with fighter phenotype can
have negative pleiotropic effects on female fitness. This variant of
gender load (Rice, 1992; Arnqvist & Tuda, 2010) may compromise
population viability and make them more prone to extinction.
We used inbred lines nearly fixed for fighter or scrambler morph to
establish outbred populations enriched for fighter or scrambler genes (F
and S population respectively), each founded by the same number of
genomes to control for initial genetic diversity. These populations were
then subjected to an incremental increase in temperature (2°C per
generation) to simulate a climate change comparable to that experienced
by many species during current global warming (Parrett et al., 2018). We
find that under such environmental change, populations enriched for
fighter genes faced a significantly elevated risk of extinction.
Mortality increased with the level of thermal stress at significantly
faster rate among individuals in F populations, but males were not
disproportionately more affected than females. Our results therefore
imply that evolution of exaggerated sexual traits may have negative
pleiotropic effect on fitness of both sexes under environmental
challenge, thus increasing the risk of population extinction.